Autogenic modulation of mechanoreceptor excitability by glutamate release from synaptic-like vesicles: evidence from the rat muscle spindle primary sensory ending

被引:78
作者
Bewick, GS [1 ]
Reid, B
Richardson, C
Banks, RW
机构
[1] Univ Aberdeen, Sch Med Sci, Inst Med Sci, Aberdeen AB25 2ZD, Scotland
[2] Univ Durham, Sch Biol & Biomed Sci, Durham DH1 3LE, England
来源
JOURNAL OF PHYSIOLOGY-LONDON | 2005年 / 562卷 / 02期
关键词
D O I
10.1113/jphysiol.2004.074799
中图分类号
Q189 [神经科学];
学科分类号
071006 ;
摘要
Fifty-nanometre diameter, clear, synaptic-like vesicles (SLVs) are found in primary mechanosensory nerve terminals of vertebrate and invertebrate animals. We have investigated their role in mechanosensory function using the muscle spindle primary endings of rat Ia afferents as a model. Uptake and release of the synaptic vesicle marker FM1-43 indicated that SLVs recycle like synaptic vesicles and do so in a Ca2+-sensitive manner. Mechanical stimulation increased SLV recycling, increasing both dye uptake and release. Immunogold/electronmicroscopy showed that, like the central synaptic endings, la peripheral endings are enriched with glutamate. Moreover, exogenous glutamate enhanced stretch-induced la excitability. Enhanced excitability persisted in the presence of antagonists to the commonest ionotropic and metabotropic glutamate receptors (kynurenate, MCPG, CPPG and MAP4). However, excitation by glutamate was abolished by (R,S)-3,5-dihydroxyphenylglycine (DHPG), and rather more effectively by (2R,1'-S,2'-R,3'-S)-2-(2'-carboxy-3'-phenylcyclopropyl) glycine (PCCG-13). PCCG-13 also significantly reduced stretch-activated excitability in the absence of exogenous glutamate. These data indicate that SLVs recycle at rest, releasing glutamate, and that mechanical activity increases this process. The blockade with DHPG and PCCG-13 suggests that endogenous glutamate release acts, at least in part, through the recently described phospholipase D-linked metabotropic Glu receptor to maintain the excitability of the sensory endings.
引用
收藏
页码:381 / 394
页数:14
相关论文
共 53 条
[1]   FINE STRUCTURE OF SENSORY REGION OF CAT MUSCLE SPINDLES [J].
ADAL, MN .
JOURNAL OF ULTRASTRUCTURE RESEARCH, 1969, 26 (3-4) :332-&
[2]   Syntaxin 1A and 1B display distinct distribution patterns in the rat peripheral nervous system [J].
Aguado, F ;
Majo, G ;
Ruiz-Montasell, B ;
Llorens, J ;
Marsal, J ;
Blasi, J .
NEUROSCIENCE, 1999, 88 (02) :437-446
[3]  
Akoev GN, 1988, MECHANORECEPTORS THE
[4]  
Albani-Torregrossa S, 1999, MOL PHARMACOL, V55, P699
[5]  
Banks RW, 2002, ADV EXP MED BIOL, V508, P13
[6]  
BANKS RW, 2000, J PHYSL, V528
[7]   OPTICAL ANALYSIS OF SYNAPTIC VESICLE RECYCLING AT THE FROG NEUROMUSCULAR-JUNCTION [J].
BETZ, WJ ;
BEWICK, GS .
SCIENCE, 1992, 255 (5041) :200-203
[8]   ACTIVITY-DEPENDENT FLUORESCENT STAINING AND DESTAINING OF LIVING VERTEBRATE MOTOR-NERVE TERMINALS [J].
BETZ, WJ ;
MAO, F ;
BEWICK, GS .
JOURNAL OF NEUROSCIENCE, 1992, 12 (02) :363-375
[9]  
BEWICK GS, 2000, J PHYSL, V528, P62
[10]  
BEWICK GS, 2004, J PHYSL, V557